Health Services Research Patient Opinions on Prostate Cancer Screening Are Swayed by the United States Preventative Services Task Force Recommendations Matthew J. Maurice and Robert Abouassaly OBJECTIVE METHODS
To survey patient opinions on prostate cancer (PCa) screening in light of the United States Preventive Services Task Force recommendation against its use. We conducted a survey of all-comers to urology and primary care clinics. Participants provided demographic information and responded to a 5-item questionnaire regarding their opinions on screening before and after reading opposing position statements. The overall response rate was 48%. After excluding incomplete questionnaires, 54 surveys were available for analysis. Patients were predominantly white, middle-aged and older, collegeeducated men with middle-to-upper-middle-class incomes who were seen at urology clinics. Patients rated their “pre” level of understanding of screening recommendations as good or very good (52%), okay (30%), and poor (19%). After reading the information sheets, good or very good understanding of screening recommendations improved (65%; P ¼ .05), and agreement with the importance of screening remained high (80%). However, nearly 20% of patients expressed a more neutral or less favorable attitude toward the risk-beneﬁt ratio of screening (P ¼ .09). Agreement that men should undergo screening, that screening helps detect cancer, and that screening saves lives remained high, regardless of the exposure. Overall, patients favor PCa screening, but heightened awareness of the current controversy raises concerns about its potential harms. PCa screening is a complex issue, and insight into changing public opinion will be crucial to our future discussions with patients who are wrestling with the decision whether to undergo screening. UROLOGY 84: 295e299, 2014. 2014 Elsevier Inc.
n May 2012, the United States Preventative Services Task Force (USPSTF) ﬁnalized its recommendation to discontinue prostate-speciﬁc antigen (PSA)-based screening for prostate cancer (PCa) screening in all men, regardless of age, citing its unfavorable risk-beneﬁt ratio.1 Although the long-term impact of this new recommendation on men’s health outcomes is unclear, its effect on practice patterns is evident. In response, there is evidence of decreased PSA testing by primary care physicians.2 In contrast, the American Urological Association (AUA) has upheld the use of selective PSA screening in age-appropriate men who have come to the decision after a thorough discussion with their physicians.3 Similarly, Financial Disclosure: The authors declare that they have no relevant ﬁnancial interests. From the Urology Institute, University Hospitals Case Medical Center, Case Western Reserve University School of Medicine, Cleveland, OH An abstract of the work was presented at the annual meeting of the North Central Section of the American Urological Association in Naples, Florida on October 10, 2013. Reprint requests: Robert Abouassaly, M.D., M.S., Urology Institute, University Hospitals Case Medical Center, Case Western Reserve University School of Medicine, 11100 Euclid Avenue, Cleveland, OH 44106. E-mail: [email protected]
org Submitted: February 17, 2014, accepted (with revisions): April 15, 2014
ª 2014 Elsevier Inc. All Rights Reserved
the American Cancer Society and the American Society of Clinical Oncology support a shared decision-making strategy, wherein men have the opportunity to make an informed decision with their physicians about whether to be screened for PCa.4,5 In light of these conﬂicting recommendations, the decision whether to screen or be screened for PCa is confusing, even for health care providers,6 and increasing responsibility is being placed on patients to participate in this decision-making process.3-5 Unfortunately, little is known about contemporary patient opinions on PCa screening. Furthermore, patients’ awareness of and response to the new recommendations has not been studied. To aid our future discussions with patients, we sought to better understand their opinions on PCa screening before and after exposure to the updated 2012 USPSTF and AUA guidelines.
MATERIALS AND METHODS We conducted an anonymous survey of adult (18 years) patients presenting to urology and primary care clinics at our institution over a 4-month period (March 2013-July 2013). http://dx.doi.org/10.1016/j.urology.2014.04.026 0090-4295/14
Figure 1. Information on prostate cancer screening, based on online patient education materials from the American Urological Association.
A total of 200 surveys were distributed at participating clinics in a 1:8 ratio between primary care and urology clinics. Patients belonging to vulnerable groups (ie, decisionally impaired patients, prisoners, and family members of the research team) were excluded. The survey consisted of a demographic questionnaire followed by a 5-item “pre” questionnaire asking about baseline opinions on PCa screening. Patients were then exposed to 2 separate anonymized information sheets, which summarized the AUA (Fig. 1) and USPSTF (Fig. 2) interpretations of the data on PCa screening. The information sheets were adapted from patient handout sheets and position statements available on the USPSTF and AUA websites at the time of survey creation. In keeping with their respective biases, the USPSTF-like handout presented PSA screening in a negative light, whereas the AUA-like handout presented it in a more neutral light. After the exposure, patients were asked to complete a 5-item “post” questionnaire, identical to the one completed at the survey onset. The survey was developed with a Flesch-Kincaid reading level of eighth grade or below. Participation in the survey was optional, and patients were asked to return the survey even if it was not completed. Completing the survey more than once was discouraged. Institutional review board approval was obtained before study initiation.
Only fully completed surveys with responses to all “pre” and “post” questionnaires were analyzed. Partially completed and blank surveys were excluded. Survey responses were expressed as percentages. To compare baseline characteristics (categorical variables) of the participants from the included and excluded surveys, chi square tests were used. Matched “pre” and “post” responses were analyzed using the Bhapkar test for marginal homogeneity to determine if the distribution of responses changed following exposure to the information sheets.7 P values <.05 were considered statistically signiﬁcant. All statistical tests were performed using SAS, version 9.3 (SAS Institute Inc., Cary, NC).
RESULTS Ninety-ﬁve completed or partially completed surveys were returned, yielding a 48% overall response rate. Forty surveys were excluded because the “post” questionnaire was unanswered or incomplete. A single additional survey was excluded because the “pre” questionnaire was incomplete. After exclusion, there were a total of 54 surveys (57%) available for analysis. The baseline characteristics of excluded patients did not differ signiﬁcantly from those of patients included in the analysis (Table 1).
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Figure 2. Information on prostate cancer screening, based on online patient education materials from the United States Preventative Services Task Force.
Included patients were predominantly aged 55 years (37 of 51; 73%), Caucasian (43 of 50; 86%), and male (48 of 51; 94%). Seventeen of 51 patients (33%) were college educated, and 27 of 45 (60%) earned $60,000 per year. Forty-eight of 54 patients (89%) were seen at urology clinics at the time of the survey (Table 1). At baseline, 28 of 54 patients (52%) reported a good or very good understanding of PCa screening recommendations. Patients expressed strong support for PCa screening, agreeing that it increases PCa detection and improves PCa survival. Most patients (34 of 54; 63%) disagreed that the risks of screening outweigh the beneﬁts (Table 2). In response to the USPSTF- and AUA-modeled information handouts, overall understanding of screening recommendations increased by 17% (9/54), which approached signiﬁcance (P ¼ .05). Other nonsigniﬁcant trends were noted. Support for routine PCa screening waned, from 47 of 54 (87%) “pre” to 43 of 54 (80%) “post”, with most of these patients developing a strong opposition to screening (P ¼ .60). In addition, fewer patients were certain that screening confers a survival beneﬁt, from 46 of 54 (85%) “pre” to 42 of 54 (78%) UROLOGY 84 (2), 2014
“post” (P ¼ .60). Lastly, 7 of 54 patients (13%) changed their minds, adopting a less favorable opinion toward the risk-beneﬁt ratio of PCa screening (P ¼ .09). Alternatively, the belief that screening increases PCa detection did not change signiﬁcantly among patients (P ¼ .88).
COMMENT Amidst the negative press that PSA screening has received in recent years, little is known about contemporary patient opinions on PCa screening.1,8 In an effort to facilitate our discussions with patients about screening, we sought to better understand our patients’ baseline knowledge of the current screening controversy and to determine their response to the conﬂicting data put forth by the AUA and USPSTF, in support of and in opposition to PSA screening, respectively. At baseline, 52% patients reported a good grasp of PCa screening recommendations, and nearly 90% generally supported screening. After being presented with handouts echoing the AUA and USPSTF positions, 17% of patients reported improved understanding. 297
Table 1. Baseline participant characteristics Variables Survey site Urology clinic Gender Male Age, y 18-34 35-54 55-74 75 Race White Black Other Highest education Less than high school High school College Professional Household income <$30,000 $30,000-$59,999 $60,000-$99,999 $100,000
Included, N (%)
Excluded, N (%)
4 10 34 3
1 9 18 10
P Value* .83 .14 .06
(8) (20) (67) (6)
(2.6) (24) (47) (26) .22
43 (86) 5 (10) 2 (4)
27 (73) 5 (14) 5 (14)
1 24 17 9
(2) (47) (33) (18)
5 16 13 3
(14) (43) (35) (8)
9 9 10 17
(20) (20) (22) (38)
12 9 8 5
(35) (27) (24) (15)
P values <.05 considered signiﬁcant. * Chi square test.
Although this change approached statistical signiﬁcance (P ¼ .05), the sample size may have been too small to detect a difference. In addition, approximately 10% of these patients, who presumably had been unaware of the most recent grade-D recommendation by the USPSTF, expressed a less favorable opinion toward screening after the exposure. Speciﬁcally, participants were concerned by the limited survival beneﬁt and unfavorable riskbeneﬁt ratio of screening. Interestingly, patients consistently agreed that screening increases cancer detection, with no signiﬁcant difference in “pre” and “post” responses. Altogether, these results raise concerns that the USPSTF recommendations may deter age-appropriate men from discussing screening with their physicians in the future. To our knowledge, we are the ﬁrst to examine contemporary patient opinions on PCa screening since the release of the 2012 USPSTF recommendation, which categorically discouraged PSA screening. In the past, the public has not supported initiatives to discontinue or minimize PCa screening. According to Caire et al,9 78% of men disagreed with the 2008 USPSTF recommendation to discontinue PSA screening in men aged 75 years. In a similar fashion, we found that 80% of our patients continued to support PCa screening, even after reading about its limitations. Despite their overwhelming support for screening, our patients did seem to be receptive to the potential harms and the potentially limited beneﬁts of screening. Aside from its novelty, our study is highly applicable to current urology practice. Our patients were predominantly middle-aged and older men seen at urology clinics. 298
Although these patients may not represent the general public or men seeking general health maintenance, our study population is highly representative of general urology patients. This population is clinically relevant because it represents men who are eligible for PSA screening and who may require counseling on screening in the future. The AUA urges age-appropriate men to discuss the beneﬁts and harms of screening with their physicians.3 As we move toward a policy of targeted screening based on shared decision-making, it will be vitally important to understand patients’ pre-existing biases toward screening and to have decision support tools available to assist them in deciding whether to be screened.10,11 With primary care physicians abandoning the practice of screening in accordance with current medical guidelines, the responsibility to discuss the appropriateness of screening with patients will fall largely on urologists.1,2 In light of our ﬁndings, informed patients seem to be less supportive of screening and may be more hesitant to broach the topic with health care providers. In turn, urologists may need to be more proactive in initiating this dialog, despite the mounting time constraints on busy practitioners. Patient decision aids, like the ones we adapted, which express the beneﬁts and harms of screening in a fair and balanced way, have been shown to be very useful for educating patients in clinical practice.11 In fact, the use of informational handouts also proved to be informative for patients in our study, allowing them to interpret the conﬂicting data and opposing viewpoints on screening and to formulate their own informed opinions on the matter. This is evidenced by the fact that patients upheld the notion that screening increases cancer detection, although they adopted new opinions on the survival beneﬁt and risk-beneﬁt ratio of screening. This response suggests informed decision-making, that is, patients came to a decision after acknowledging and weighing the risks and beneﬁts of screening. Patient handouts, like the ones we provided, may facilitate and expedite discussions on screening in other populations as well. There are limitations to our study worth noting. We recognize several sources of potential bias that may threaten the validity of our results. As with any survey, our study suffers from self-selection bias. Although our overall response rate was acceptable (48%), we introduced the potential for additional selection bias by excluding incomplete surveys from our analysis. As our ﬁnal study population did not differ signiﬁcantly from the excluded sample, our results should retain internal validity. It is possible, however, that the 41 surveys that were excluded due to incompleteness may have been incomplete because of the inability of participants to arrive at conclusions about screening on their own. Although more than half of these surveys were fully incomplete suggesting insufﬁcient time for completion rather than impaired decision-making ability, it is possible that some patients may require more time and/or more physician-led guidance to make these difﬁcult decisions. By primarily surveying patients who were being seen at urology clinics, we also introduced UROLOGY 84 (2), 2014
Table 2. Patient opinions on prostate cancer screening preinformational and postinformational handouts Questions
Pre (n ¼ 54)
Post (n ¼ 54)
1. What is your understanding of the recommendations for prostate cancer screening? Good/very good 28 52 37 69 Okay 16 30 14 26 Poor/very poor 10 19 3 6 2. Men should be routinely screened for prostate cancer. Agree/strongly agree 47 87 43 80 Neutral/no opinion 7 13 8 15 Disagree/strongly disagree 0 0 3 6 3. Prostate cancer screening helps ﬁnd cancer. Agree/strongly agree 48 89 47 87 Neutral/no opinion 6 11 6 11 Disagree/strongly disagree 0 0 1 2 4. Prostate cancer screening saves lives. Agree/strongly agree 46 85 42 78 Neutral/no opinion 8 15 10 19 Disagree/strongly disagree 0 0 2 4 5. Prostate cancer screening causes more harm than good. Agree/strongly agree 9 17 13 24 Neutral/no opinion 11 20 14 26 Disagree/strongly disagree 34 63 27 50
17 4 13
7 2 6
2 0 2
7 4 4
7 6 13
P values <.05 considered signiﬁcant. * A positive value indicates a more favorable “post” response, whereas a negative value indicates a less favorable “post” response. y The Bhapkar test for marginal homogeneity was used to test for a difference in the matched “pre” and “post” responses to each question.
sampling bias into our study that may affect its generalizability. As discussed previously, this was an intended consequence of preferentially surveying urology clinics. Finally, because our survey was conducted after the release of the newest USPSTF recommendations, prior awareness of these recommendations may have inﬂuenced responses, especially the high baseline level (52%) of understanding of screening recommendations. Although it is unlikely that all of these patients were aware of the USPSTF gradeD recommendation at the time of the survey, the results of our baseline analysis reﬂect the attitudes of, at best, a partially informed cohort. Consequently, this pre-existing knowledge may have diminished the magnitude of the pre- and-post-exposure effect.
CONCLUSIONS In general, PCa screening is strongly supported by patients. In response to the new USPSTF recommendations, support for PCa screening remains high, but there is a greater appreciation for its potential harms. An informed patient population that is aware of the controversy surrounding PCa screening seems better equipped to grasp this complex issue. Decision-making tools that provide fair and balanced information on PCa screening recommendations may facilitate future patient discussions on the topic. References 1. Moyer VA, LeFevre ML, Sui AL, et al. Screening for prostate cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2012;157:120-134.
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2. Aslani A, Minnillo BJ, Johnson B, et al. The impact of recent screening recommendations on prostate cancer screening in a large health care system [e-pub ahead of print]. J Urol. doi: 10.1016/j.juro. 2013.12.010, accessed December 15, 2013. 3. Carter HB, Albertsen PC, Barry MJ, et al. Early detection of prostate cancer: AUA Guideline. J Urol. 2013;190:419-426. 4. Basch E, Oliver TK, Vickers A, et al. Screening for prostate cancer with prostate-speciﬁc antigen testing: American Society of Clinical Oncology Provisional Clinical Opinion. J Clin Oncol. 2012;30: 3020-3025. 5. Smith RA, Brooks D, Cokkinides V, et al. Cancer screening in the United States, 2013: a review of current American Cancer Society guidelines, current issues in cancer screening, and new guidance on cervical cancer screening and lung cancer screening. CA Cancer J Clin. 2013;63:88-105. 6. Hoag NA, So AI. The confusion surrounding prostate cancer screening faced by family physicians. Can Urol Assoc J. 2012;6: 194-195. 7. Sun X and Yang Z: Generalized McNemar’s test for homogeneity of the marginal distributions: Paper 382-2008. Paper presented at: SAS Global Forum. March 16-19, 2008; San Antonio, TX. Available at: http://www2.sas.com/proceedings/forum2008/382-2008.pdf. Accessed December 15, 2013. 8. Calonge N, Petitti DB, DeWitt TG, et al. U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149: 185-191. 9. Caire AA, Sun L, Robertson CN, et al. Public survey and survival data do not support recommendations to discontinue prostatespeciﬁc antigen screening in men at age 75. Urology. 2010;75: 1122-1127. 10. Carter HB. American Urological Association (AUA) guideline on prostate cancer detection: process and rationale. BJU Int. 2013;112: 543-547. 11. Lin GA, Aaronson DS, Knight SJ, et al. Patient decision aids for prostate cancer treatment: a systematic review of the literature. CA Cancer J Clin. 2009;59:379-390.